Laparoscopic versus open adhesiolysis in patients with adhesive small bowel obstruction: a systematic review and meta-analysis

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1 The American Journal of Surgery (2012) 204, Review Article Laparoscopic versus open adhesiolysis in patients with adhesive small bowel obstruction: a systematic review and meta-analysis Ming-Zhe Li, M.D. a,1, Lei Lian, M.D. b,1, Long-bin Xiao, M.D. a, Wen-hui Wu, M.D. a, Yu-long He, M.D. a, Xin-ming Song, M.D. a, * a Department of Gastrointestinal and Pancreatic Surgery, the First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China ; b Department of Colorectal Surgery, the Sixth Affiliated Hospital (Gastrointestinal Hospital), Sun Yat-sen University, Guangzhou, China KEYWORDS: Adhesiolysis; Laparoscopic; Meta-analysis; Smallbowel obstruction Abstract BACKGROUND: The objective of this study was to evaluate whether surgical outcomes differ between laparoscopy versus the open approach for adhesive small bowel obstruction. METHODS: PubMed, MEDLINE, Embase, and the Cochrane Library databases were electronically searched from 1985 to The study pooled the effects of outcomes of a total of 334 patients enrolled into 4 retrospective comparative studies using meta-analytic methods. RESULTS: Laparoscopic adhesiolysis was associated with a reduced overall complication rate (odds ratio.42,.25.70, P.01), prolonged ileus rate (odds ratio.28,.10.73, P.01) and pulmonary complication rate (odds ratio.20,.04.94, P.04) compared with the open approach. No significant differences were noted for intraoperative injury to bowel rates (odds ratio 1.93, , P.17), wound infection rates (odds ratio.44, , P.08), and mortality (odds ratio.81, , P.83). CONCLUSIONS: Laparoscopic adhesiolysis is advantageous in most of the analyzed outcomes. Laparoscopic treatment of small bowel obstruction is recommended by experienced laparoscopic surgeons in selected patients Elsevier Inc. All rights reserved. Postoperative adhesions account for 74% of small bowel obstructions. 1 Open adhesiolysis has been the main treatment for patients with adhesive bowel obstruction requiring surgery. However, laparotomy is associated with disruption to the visceral peritoneum, which predisposes the patients to more adhesions and results in further bowel obstruction. Moreover, 1 Authors Ming-Zhe Li and Lei Lian contributed equally to this paper. * Corresponding author. Tel: ; fax: address: songxm2010@163.com Manuscript received November 3, 2011; revised manuscript March 4, 2012 about 10% to 30% of patients suffer recurrent bowel obstruction after the initial open adhesiolysis and require repeat surgery. 2 4 After Bastug performed the first successful laparoscopic adhesiolysis for small bowel obstruction in 1991, 5 laparoscopic adhesiolysis has been increasingly accepted by more and more surgeons because of its fewer intra-abdominal adhesions, low morbidity, shorter hospital stay, and faster recovery. 6,7 Some trials have shown the safety of laparoscopic adhesiolysis for adhesive small bowel obstruction However, scant data exist on the safety of laparoscopy for adhesive small bowel obstruction, and the results are conflicting. The aim of this /$ - see front matter 2012 Elsevier Inc. All rights reserved.

2 780 The American Journal of Surgery, Vol 204, No 5, November 2012 Figure 1 The article selection flow chart. study was to compare laparoscopic and open adhesiolysis for small bowel obstruction using a meta-analysis. Materials and Methods Search and selection strategies PubMed, MEDLINE, Embase, and the Cochrane Library databases between January 1985 and June 2010 were electronically searched for laparoscopy, laparoscopic, and adhesion with obstruction. In addition, the references of relevant studies were hand searched for further studies that may have been missed. The most recent search was performed in July Inclusion criteria and exclusion criteria All randomized controlled trials, retrospective cohort studies, and comparative studies investigating laparoscopic versus Table 1 Characteristics of the trials included in this study First author Year Study type Sample size Conversion rate (%) Intestinal resection rate Independent variables Prior procedures Wullstein Retrospective matched-pair analysis Chopra Retrospective observational study Khaikin Retrospective matched-pair analysis Grafen Retrospective observational study LAP n 52 Open n 52 LAP n 34 Open n 41 LAP n 31 Open n 31 LAP n 90 Open n LAP: 7.7 NS between groups: age, sex, number of previous laparotomies, and duration of symptoms 32.4 LAP: 13.3 NS between groups: age Open: LAP: 25.8 Open: 32.3 NS between groups: BMI, ASA score, previous surgery, previous episodes of SBO 26.0 LAP: 8.0 SS between groups: lower preoperative ASA scores in the LAP group NS between groups: age, sex, and preoperative laboratory tests Appendectomies, gynecologic, cholecystectomy, colonic resection, etc Not reported Appendectomies, gynecologic, colon, small bowel, multiple operations. etc Appendectomy, cholecystectomy, etc LAP laparoscopic; ASA American Society of Anesthesiologists; SBO small bowel obstruction; BMI body mass index; SS statistically significant; NS statistically nonsignificant.

3 M.-Z. Li et al. Meta-analysis of laparoscopic adhesiolysis 781 Table 2 Methodologic qualities of retrospective cohort studies Quality variables Wullstein et al 12 Chopra et al 13 Khaikin et al 14 Inclusion criteria Exclusion criteria Demographics comparable Can the number of participating centers be determined Can the number of surgeons who participated be determined Can the reader determine where the authors are on the learning curve for the reported procedure Are diagnostic criteria clearly stated for clinical outcomes if required Is the surgical technique adequately described Is there any way that they have tried to standardize the operative technique Is there any way that they have tried to standardize perioperative care Is the age and range given for patients in the laparoscopic group Do authors address whether any data are missing Is the age and range given for patients in the open group Were patients in each group treated along similar timelines Did all the patients asked to enter the study take part Dropout rates stated Outcomes clearly defined Blind assessors Standardized assessment tools Analysis by intention to treat Score Total 20: less than, 8 poor quality; 8 14, fair quality; 15 or more, good quality. Data from the Scottish Intercollegiate Guidelines Network, Rangel et al, 18 and Sajid et al. 19 Grafen et al 15 open surgery for adhesive small bowel obstruction were identified. Trials on patients of any age and sex published in English were included. Authors with more than 1 published study were represented by their most recent publication to avoid multiple reporting of patients. Studies were excluded if they (1) did not compare laparoscopic with open surgery, (2) were in a language for which a translation to English was not available, or (3) were unpublished studies or abstracts presented at national and international meetings. Methods of review Each article was critically reviewed by 2 researchers (M.Z. and L.L.) independently using the double extraction method for eligibility by our inclusion criteria and confirmed by a third researcher (X.M.). All conflicts were discussed and resolved before the final analysis. The outcome measures were the overall complication rate, the intraoperative injury to bowel rate, the wound infection rate, the prolonged ileus rate, the pulmonary complication rate, and mortality. Complications included intraoperative and postoperative morbidities such as perforation, hemorrhage, injury to the mesentery, wound infection, anastomotic leakage, and pneumonia. The laparoscopic group comprised all patients for whom laparoscopy was intended including those whose operation was converted, and the open group comprised patients who underwent laparotomy for adhesiolysis. Statistical analysis Statistical analysis was performed on the studies for the overall complication rate, the intraoperative injury to bowel rate, the wound infection rate, the prolonged ileus rate, the pulmonary complication rate, and mortality for laparoscopic versus open adhesiolysis in patients with adhesive small bowel obstruction. The level of statistical significance was set at P.05. Heterogeneity was quantified by calculating I 2 where P.10 was determined to be significant. For dichotomous data, results were expressed as an odds ratio (OR) with the 95% confidence interval (CI). ORs were calculated using fixed-effects models for each outcome. Publication bias was evaluated using a funnel plot. The meta-analysis was executed on RevMan 5.0 software (Cochrane-Information and Management System, The Nordic Cochrane Centre, the Cochrane Collaboration, Copenhagen). The type 2 statistical error ( ) was calculated by

4 782 The American Journal of Surgery, Vol 204, No 5, November 2012 Figure 2 A funnel plot showing no significant publication bias. Power and Sample Size Program software 3.0 (Copyright by William D. Dupont and Walton D. Plummer, Vanderbilt University School of Medicine, USA). Results Article search The initial literature search identified 105 studies. Based on the inclusion criteria, 94 studies were excluded, with a selection of 11 studies for more detailed review. Seven of those studies were subsequently excluded (Fig. 1) including 6 retrospective case series studies and 1 serious methodologic flaw with a high bias risk directly affecting the outcome, 16 leaving 4 retrospective observational/case-controlled studies for meta-analysis. Characteristics of each trial are given in Table 1. The conversion rate ranged from 26% to 51.9%. Procedures performed before the episode of bowel obstruction included appendectomy, gynecologic operations, cholecystectomy, and colonic resection (Table 1). Methodologic quality of included studies The methodologic quality of the included trials is explained comprehensively in Table 2. The allocation concealment and the blinding of the investigator or assessor were not clearly reported in all the trials. Therefore, the results of this review might be biased. Based on Scottish Intercollegiate guidelines Network, 17 Rangel et al, 18 and Sajid et al, 19 all the trials were considered to be of fair quality. In addition, no publication bias between the studies was observed (Fig. 2). Overall complication All 4 studies reported perioperative complications An approximately equal number of complications was observed in the 2 groups. There was a statistically significant reduction in the overall complication rate in the laparoscopic group compared with the open group (OR.42; 95% CI,.25.70; z 3.29; P.01). Figure 3 shows a forest plot for overall complications. The test for heterogeneity was not statistically significant (I 2 25%, P.26). Figure 3 A forest plot showing the overall complications between laparoscopy and open adhesiolysis for patients with adhesive small bowel obstruction requiring surgery. LAP, laparoscopic group.

5 M.-Z. Li et al. Meta-analysis of laparoscopic adhesiolysis 783 Figure 4 A forest plot showing intraoperative injury to the bowel between laparoscopy and open adhesiolysis for patients with adhesive small bowel obstruction requiring surgery. LAP, laparoscopic group. Intraoperative bowel injury Two studies reported intraoperative bowel injury. 12,15 The number of intraoperative bowel injuries varied from 0 to 15. Overall, the total number of intraoperative bowel injuries was 16 in the laparoscopic group and 8 in the open group. No statistically significant difference was noted in the number of intraoperative bowel injuries between the 2 groups (OR 1.93; 95% CI, ; z 1.39; P.17). The type 2 statistical error ( ) was.675. The test for heterogeneity was not statistically significant (I 2 63%, P.10). Figure 4 shows a forest plot for intraoperative injuries to the bowel between the laparoscopic and open groups. Wound infection Three studies reported wound infections A forest plot showing wound infection as a complication is shown in Figure 5. Overall, 7 wound infections were noted in the laparoscopic group and 16 wound infections in the open group. No statistically significant difference was observed for wound infections between the laparoscopic and open groups (OR.44; 95% CI, ; z 1.73; P.08). The type 2 statistical error ( ) was.57. The test for heterogeneity was not statistically significant (I 2 10%, P.33). Prolonged ileus Only 2 studies reported data on prolonged ileus, and significant heterogeneity was present among the studies (I 2 70%, P.07). 13,14 There was a statistically significant reduction in prolonged ileus in the laparoscopic group compared with the open group (OR.28; 95% CI,.10.73; z 2.58; P.01). Figure 6 shows a forest plot for prolonged ileus between the laparoscopic and open groups. Pulmonary complications Pulmonary complications were measured in 3 studies, and there was no significant heterogeneity among the studies A meta-analysis of data from the 3 studies showed a significant difference between the 2 procedures (OR.20; 95% CI,.04.94; z 2.04; P.04). The test for heterogeneity was not statistically significant (I 2 0, P.70). Figure 7 shows a forest plot for pulmonary complications between the laparoscopic and open groups. Mortality Only 2 studies provided data on mortality. 13,15 Significant heterogeneity was present among the studies (I 2 67%, P.08). There was no significant difference between the 2 procedures with respect to the overall mortality (OR.81; 95% CI, ; z.22; P.83). The type 2 statistical error ( ) was.94. Figure 8 shows a forest plot describing the overall mortality between the laparoscopic and open groups. Comments Although laparotomy may cause adhesion in the abdominal cavity, open adhesiolysis has traditionally been the Figure 5 A forest plot showing wound infection between laparoscopy and open adhesiolysis for patients with adhesive small bowel obstruction requiring surgery. LAP, laparoscopic group.

6 784 The American Journal of Surgery, Vol 204, No 5, November 2012 Figure 6 A forest plot showing prolonged ileus between laparoscopy and open adhesiolysis for patients with adhesive small bowel obstruction requiring surgery. LAP, laparoscopic group. main treatment for patients with adhesive small bowel obstruction. Because of the difficulty in establishing a working space and visualizing the site of obstruction and the risk of injury to the distended bowel, laparoscopic adhesiolysis for small bowel obstruction was considered inappropriate for intestinal adhesion in the past. With increasing experience in laparoscopic adhesiolysis after Bastug in 1991, the reported success rate ranged from 46% to 87% However, the safety of laparoscopic surgery in the treatment of adhesive small bowel obstruction is still unclear because there are only a few reports showing its safety and there are no randomized controlled trials comparing open with laparoscopic adhesiolysis. 8,26 The aim of this meta-analysis was to summarize current evidence with regard to laparoscopic and open adhesiolysis in the management of patients with adhesive small bowel obstruction. Overall, the quality of the studies found was intermediate without significant heterogeneity. In this study, a meta-analysis of these 4 retrospective studies showed that laparoscopic adhesiolysis was advantageous to open surgery in terms of the overall complication rate, the prolonged ileus rate, and the pulmonary complication rate. Moreover, there was no significant difference between the 2 procedures with respect to intraoperative bowel injury, wound infection rate, and mortality. It showed laparoscopic adhesiolysis was a safe treatment for adhesive small bowel obstruction with a short-term follow-up. However, it is important to note that all the outcomes measured for assessing the efficacy of laparoscopy against open adhesiolysis in patients with adhesive small bowel obstruction in the studies included were based on a short-term follow-up. Important measurement outcomes including the costs as well as other life quality issues, such as the time to return to normal daily activities and work and cosmesis, were not addressed. In addition, a long-term follow-up of patients including the recurrence rate is lacking, and complications such as hernias and intestinal obstruction lack evaluation. Furthermore, none of these studies have addressed the issue regarding recurrent bowel obstruction after open or laparoscopic adhesiolysis. This issue is important because it might be the most valid outcome measurement when comparing laparoscopic versus open approach in this particular clinical scenario. In the present study, higher bowel injury rates in the laparoscopic group with a high type 2 statistical error (.675) should be more carefully considered although they are not statistically significant. Suter et al 26 also reported a higher rate of bowel injury in the laparoscopic group. Possible reasons why laparoscopic surgery was associated with a higher rate of intraoperative bowel injury were a severe adhesion was involved, inexperience, and impaired tactile feedback during laparoscopic manipulation. Therefore, extra care should be taken while performing laparoscopic adhesiolysis for small bowel obstruction with a known adhesion. Large sample size clinical trials with high statistical power are needed to provide more reliable evidence. The success of the laparoscopic approach depended on several factors. Suter et al 26 reported that the duration of surgery and a bowel diameter exceeding 4 cm were predictors of conversion. Levard et al 27 showed that the rate of success was significantly higher in patients operated on early ( 24 hours after hospitalization vs 48 hours) and who had only 1 or 2 prior operations or who had single band Figure 7 A forest plot showing pulmonary complications between laparoscopy and open adhesiolysis for patients with adhesive small bowel obstruction requiring surgery. LAP, laparoscopic group.

7 M.-Z. Li et al. Meta-analysis of laparoscopic adhesiolysis 785 Figure 8 A forest plot showing the overall mortality between laparoscopy and open adhesiolysis for patients with adhesive small bowel obstruction requiring surgery. LAP, laparoscopic group. obstruction rather than diffuse adhesions. Early operation after the onset of symptoms as well as after hospitalization was an important success factor, probably because intestinal distension and necrosis were found less frequently. Grafen et al 15 found that patients with adhesive small bowel obstruction who previously had undergone appendectomy or cholecystectomy alone could all be successfully managed laparoscopically. This may because of the simplicity of the adhesions encountered in patients after minor operations such as an appendectomy or cholecystectomy. Therefore, an attempt at laparoscopic management of acute adhesive small bowel obstruction seems justified in patients who are seen early and who have had fewer than 2 previous laparotomies. Bailey et al 28 showed that the surgeon s experience was a major factor on successful laparoscopic adhesiolysis. Needless to say, experience in advanced laparoscopic surgery appeared advisable for the treatment of patients with more extensive adhesion formation. Therefore, laparoscopic treatment of small bowel obstruction was recommended by experienced laparoscopic surgeons in selected patients. The shortcomings of the present study are as follows. First, all the studies available for this meta-analysis were retrospective and nonrandomized studies with evident selection bias with regard to the adoption of the operative approach. However, the scarcity of randomized controlled trials is the reason why this meta-analysis is implemented. Randomized controlled trials may never be performed because of the difficulty of conducting one. Second, as we know, successful laparoscopic adhesiolysis depends on the individual surgeon s experience in laparoscopic surgery. In our study, surgeons with varying expertise were from different clinical centers. Therefore, the overall complication rate might be affected. However, intersurgeon variability is a problem that most of the clinical trials might encounter, and it is difficult to solve. Third, there was a great variation in study design in the published literature. Some studies divided the patients into intent laparoscopic, completely laparoscopic, and open groups, whereas other studies divided them into laparoscopic, converted, and open groups. Finally, this study might be underpowered. Upper confidence limits for the ORs do leave open the possibility that associations might exist. Conclusions Laparoscopic adhesiolysis is safer than the open approach because there are less overall complications, prolonged ileus rates, and pulmonary complications associated with its use. Laparoscopic treatment of small bowel obstruction is recommended by experienced laparoscopic surgeons in selected patients. Further randomized clinical trials are needed to ensure more robust conclusions. References 1. Miller G, Boman J, Shrier I, et al. Etiology of small bowel obstruction. Am J Surg 2000;180: Barkan H, Webster S, Ozeran S. Factors predicting the recurrence of adhesive small-bowel obstruction. Am J Surg 1995;170: Landercasper J, Cogbill TH, Merry WH, et al. Long-term outcome after hospitalization for small-bowel obstruction. Arch Surg 1993;128: Mucha P Jr. Small intestinal obstruction. Surg Clin North Am 1987; 67: Bastug DF, Trammell SW, Boland JP, et al. Laparoscopic adhesiolysis for small bowel obstruction. Surg Laparosc Endosc 1991;1: Tittel A, Treutner KH, Titkova S, et al. Comparison of adhesion reformation after laparoscopic and conventional adhesiolysis in an animal model. Langenbecks Arch Surg 2001;386: Tsao KJ, St Peter SD, Valusek PA, et al. Adhesive small bowel obstruction after appendectomy in children: comparison between the laparoscopic and open approach. J Pediatr Surg 2007;42: Strickland P, Lourie DJ, Suddleson EA, et al. Is laparoscopy safe and effective for treatment of acute small-bowel obstruction? Surg Endosc 1999;13: Lee IK, Kim do H, Gorden DL, et al. Selective laparoscopic management of adhesive small bowel obstruction using CT guidance. Am Surg 2009;75: Chowbey PK, Panse R, Sharma A, et al. Elective laparoscopy in diagnosis and treatment of recurrent small bowel obstruction. Surg Laparosc Endosc Percutan Tech 2006;16: Liauw JJ, Cheah WK. Laparoscopic management of acute small bowel obstruction. Asian J Surg 2005;28: Wullstein C, Gross E. Laparoscopic compared with conventional treatment of acute adhesive small bowel obstruction. Br J Surg 2003;90: Chopra R, McVay C, Phillips E, et al. Laparoscopic lysis of adhesions. Am Surg 2003;69: Khaikin M, Schneidereit N, Cera S, et al. Laparoscopic vs. open surgery for acute adhesive small-bowel obstruction: patients outcome and cost-effectiveness. Surg Endosc 2007;21: Grafen FC, Neuhaus V, Schöb O, et al. Management of acute small bowel obstruction from intestinal adhesions: indications for laparo-

8 786 The American Journal of Surgery, Vol 204, No 5, November 2012 scopic surgery in a community teaching hospital. Langenbecks Arch Surg 2010;395: Mancini GJ, Petroski GF, Lin WC, et al. Nationwide impact of laparoscopic lysis of adhesions in the management of intestinal obstruction in the US. J Am Coll Surg 2008;207: Methodology Checklist: cohort studies. SIGN. Available at: Accessed: October 1, Rangel SJ, Kelsey J, Colby CE, et al. Development of a quality assessment scale for retrospective clinical studies in pediatric surgery. J Pediatr Surg 2003;38: Sajid MS, Siddiqui MR, Baig MK. Open vs laparoscopic repair of full-thickness rectal prolapse: a re-meta-analysis. Colorectal Dis 2010; 12: Mathieu X, Thill V, Simoens Ch, et al. Laparoscopic management of acute small bowel obstruction: a retrospective study on 156 patients. Hepato Gastroenterol 2008;55: Nagle A, Ujiki M, Denham W, et al. Laparoscopic adhesiolysis for small bowel obstruction. Am J Surg 2004;187: Zerey M, Sechrist CW, Kercher KW, et al. Laparoscopic management of adhesive small bowel obstruction. Am Surg 2007;73: Ellis H, Moran BJ, Thompson JN, et al. Adhesion-related hospital readmissions after abdominal and pelvic surgery: a retrospective cohort study. Lancet 1999;353: Gutt CN, Oniu T, Schemmer P, et al. Fewer adhesions induced by laparoscopic surgery. Surg Endosc 2004;18: Sato Y, Ido K, Kumagai M, et al. Laparoscopic adhesiolysis for recurrent small bowel obstruction: long-term follow-up. Gastrointest Endosc 2001;54: Suter M, Zermatten P, Halkic N, et al. Laparoscopic management of mechanical small bowel obstruction: are there predictors of success or failure? Surg Endosc 2000;14: Levard H, Boudet MJ, Msika S, et al. Laparoscopic treatment of acute small bowel obstruction: a multicentre retrospective study. ANZ J Surg 2001;71: Bailey IS, Rhodes M, O Rourke N, et al. Laparoscopic management of acute small bowel obstruction. Br J Surg 1998;85:84 7.

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